The effects of chronic nitrate supplementation on erythrocytic methaemoglobin reduction in cattle
I. Godwin A B , L. Li A , K. Luijben A , N. Oelbrandt A , J. Velazco A , J. Miller A and R. Hegarty AA School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
B Corresponding author. Email: igodwin@une.edu.au
Animal Production Science 55(5) 611-616 https://doi.org/10.1071/AN13366
Submitted: 2 September 2013 Accepted: 6 February 2014 Published: 8 May 2014
Abstract
Calcium nitrate and urea were fed as a supplement on an isonitrogenous basis to Angus steers and their erythrocytic methaemoglobin concentrations and NADH- and NADPH-methaemoglobin reductase levels were measured over a 54-day period. Methaemoglobin concentrations remained elevated despite increases in NADH-methaemoglobin reductase activity. In a second experiment, Brahman cross steers were fed either calcium nitrate or urea supplements for 111 days. Blood cells were then taken, washed and exposed to sodium nitrite to convert all haemoglobin to methaemoglobin. The rates of glycolysis and methaemoglobin reduction were measured following incubation of these cells in buffers containing 1, 5 or 10 mM inorganic phosphate. Glucose consumption and methaemoglobin reduction were increased by inorganic phosphate and were more rapid in those animals supplemented with nitrate. Lactate production of erythrocytes was reduced in those animals fed nitrate. It is concluded that adaptation to chronic nitrite exposure occurs in the erythron, resulting in greater methaemoglobin reduction potential and that there is competition between NADH-methaemoglobin reductase and lactate dehydrogenase for NADH.
Additional keywords: inorganic phosphate, methaemoglobin reductase.
References
Agar NS, Harley JD (1972) Erythrocytic methaemoglobin reductases of various mammalian species. Experientia 28, 1248–1249.| Erythrocytic methaemoglobin reductases of various mammalian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXitlOm&md5=1829d0212a23711fd053f6e8b94d3829CAS | 4404479PubMed |
Agar NS, Godwin IR, Suzuki M, Hablethwaite J, Roberts J, Hume ID (1986) Comparative red blood cell metabolism in three wallaby species, Macropus eugenii, Macropus parma and Thylogale thetis (Macropodidae: Marsupialia). Comparative Biochemistry and Physiology Part A: Physiology 85, 297–299.
| Comparative red blood cell metabolism in three wallaby species, Macropus eugenii, Macropus parma and Thylogale thetis (Macropodidae: Marsupialia).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s%2FivFansQ%3D%3D&md5=db3c87db5c5a1e2fa364d7509d35e56aCAS |
Beutler E (1986) Red cell metabolism. Methods in Hematology 16, 57–72.
Burrows GE, Horn GW, McNew RW, Croy LI, Keeton RD, Kyle J (1987) The prophylactic effect of corn supplementation on experimental nitrate intoxication in cattle. Journal of Animal Science 64, 1682–1689.
Csallany AS, Ayaz KL (1978) Effects of nitrate, nitrite and Vitamin E on methemoglobin formation in rats. Toxicology Letters 2, 145–147.
| Effects of nitrate, nitrite and Vitamin E on methemoglobin formation in rats.Crossref | GoogleScholarGoogle Scholar |
Harris DJ, Rhodes HA (1969) Nitrate and nitrite poisoning in cattle in Victoria. Australian Veterinary Journal 45, 590–591.
Hegesh E, Gruener N, Cohen S, Bochkovsky R, Shuval HI (1970) A sensitive micromethod for the determination of methemoglobin in blood. Clinica Chimica Acta 30, 679–682.
| A sensitive micromethod for the determination of methemoglobin in blood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXltVCjtA%3D%3D&md5=7afbcdd8c225e0cfb5d0182bf8fb183cCAS |
Hulshof RB, Berndt A, Gerrits WJ, Dijkstra J, van Zijderveld SM, Newbold JR, Perdok HB (2012) Dietary nitrate supplementation reduces methane emission in beef cattle fed sugarcane-based diets. Journal of Animal Science 90, 2317–2323.
| Dietary nitrate supplementation reduces methane emission in beef cattle fed sugarcane-based diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFehsbjN&md5=96a48ee0214f4fa24c2e164cb62708e8CAS | 22287674PubMed |
Hultquist DE, Xu F, Quandt KS, Shlafer M, Mack CP, Till GO, Seekamp A, Betz AL, Ennis SR (1993) Evidence that NADPH-dependent methemoglobin reductase and administered riboflavin protect tissues from oxidative injury. American Journal of Hematology 42, 13–18.
| Evidence that NADPH-dependent methemoglobin reductase and administered riboflavin protect tissues from oxidative injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVGltg%3D%3D&md5=1dde05f25efde24379ffdf54fbdce8a6CAS | 8416288PubMed |
Janssen WJ, Dhaliwal G, Collard HR, Saint S (2004) Clinical problem-solving. Why ‘why’ matters. The New England Journal of Medicine 351, 2429–2434.
| Clinical problem-solving. Why ‘why’ matters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCrtrnM&md5=0f5b171eca69c744bebb8603357c8a2cCAS | 15575060PubMed |
Kennett EC, Ogawa E, Agar NS, Godwin IR, Bubb WA, Kuchel PW (2005) Investigation of methaemoglobin reduction by extracellular NADH in mammalian erythrocytes. The International Journal of Biochemistry & Cell Biology 37, 1438–1445.
| Investigation of methaemoglobin reduction by extracellular NADH in mammalian erythrocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Wjs7Y%3D&md5=e78e05dd2cf39a10be0a2ec562c43907CAS |
Lin M, Schaefer DM, Zhao GQ, Meng QX (2013) Effects of nitrate adaptation by rumen inocula donors and substrate fiber proportion on in vitro nitrate disappearance, methanogenesis, and rumen fermentation acid. Animal 7, 1099–1105.
| Effects of nitrate adaptation by rumen inocula donors and substrate fiber proportion on in vitro nitrate disappearance, methanogenesis, and rumen fermentation acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotlelt7w%3D&md5=b1f72c6652e1a5a342e8d5a2227ba70aCAS | 23391259PubMed |
McGrath JJ, Savage DB, Godwin IR (2013) The potential for pharmacological supply of 25-hydroxyvitamin D to increase phosphorus utilisation in cattle. Animal Production Science 53, 1238–1245.
| The potential for pharmacological supply of 25-hydroxyvitamin D to increase phosphorus utilisation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGgsrjJ&md5=f7596d378b2afda86931c57bc40da541CAS |
McKenzie RA, Rayner AC, Thompson GK, Pidgeon GF, Burren BR (2004) Nitrate–nitrite toxicity in cattle and sheep grazing Dactyloctenium radulans (button grass) in stockyards. Australian Veterinary Journal 82, 630–634.
| Nitrate–nitrite toxicity in cattle and sheep grazing Dactyloctenium radulans (button grass) in stockyards.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M3kvVenug%3D%3D&md5=341a45077d14d3cdb15f9f8b1d9ee1d0CAS | 15887389PubMed |
Nolan JV, Hegarty RS, Hegarty J, Godwin IR, Woodgate R (2010) Effects of dietary nitrate on fermentation, methane production and digesta kinetics in sheep. Animal Production Science 50, 801–806.
| Effects of dietary nitrate on fermentation, methane production and digesta kinetics in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrtbzP&md5=fec0fdf6d058f63b6cb019493a242d75CAS |
Ogawa E, Kobayashi K, Yoshiura N, Mukai J (1987) Bovine postparturient hemoglobinemia: hypophosphatemia and metabolic disorder in red blood cells. American Journal of Veterinary Research 48, 1300–1303.
Ogawa E, Kobayashi K, Yoshiura N, Mukai J (1989) Hemolytic anemia and red blood cell metabolic disorder attributable to low phosphorus intake in cows. American Journal of Veterinary Research 50, 388–392.
Pankow D, Ponsold W, Liedke MD, Gessner G, Pfordte A (1975) Adaptation of rats following sodium-nitrite-induced methemoglobinemia. Acta Biologica et Medica Germanica 34, 1205–1209.
Pinares-Patiño CS, McEwan JC, Dodds KG, Cardenas EA, Hegarty RS, Koolaard JP, Clark H (2011) Repeatability of methane emissions from sheep. Animal Feed Science and Technology 166–167, 210–218.
| Repeatability of methane emissions from sheep.Crossref | GoogleScholarGoogle Scholar |
Power GG, Bragg SL, Oshiro BT, Dejam A, Hunter CJ, Blood AB (2007) A novel method of measuring reduction of nitrite-induced methemoglobin applied to fetal and adult blood of humans and sheep. Journal of Applied Physiology 103, 1359–1365.
| A novel method of measuring reduction of nitrite-induced methemoglobin applied to fetal and adult blood of humans and sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhtr%2FM&md5=31e209a4af2d358209d1caf219743395CAS | 17615278PubMed |
Reis M, Alves CN, Lameira J, Tunon I, Marti S, Moliner V (2013) The catalytic mechanism of glyceraldehyde 3-phosphate dehydrogenase from Trypanosoma cruzi elucidated via the QM/MM approach. Physical Chemistry Chemical Physics 15, 3772–3785.
| The catalytic mechanism of glyceraldehyde 3-phosphate dehydrogenase from Trypanosoma cruzi elucidated via the QM/MM approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXislynsrw%3D&md5=0eb82911d09221b026f81b785152c498CAS | 23389436PubMed |
Roberts A, Withers P (2007) ‘StatistiXL 1.8.’ (Perth). Available at http://www.statistixl.com/default.aspx. [Verified February 2013]
Sugawara Y, Hayashi Y, Shigemasa Y, Abe Y, Ohgushi I, Ueno E, Shimamoto F (2010) Molecular biosensing mechanisms in the spleen for the removal of aged and damaged red cells from the blood circulation. Sensors 10, 7099–7121.
| Molecular biosensing mechanisms in the spleen for the removal of aged and damaged red cells from the blood circulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFCnurc%3D&md5=892755b89b92eb10e3cce62dff680121CAS | 22163593PubMed |
Takeshita M, Tamura M, Yubisui T, Yoneyama Y (1983) Exponential decay of cytochrome b5 and cytochrome b5 reductase during senescence of erythrocytes: relation to the increased methemoglobin content. Journal of Biochemistry 93, 931–934.
| Exponential decay of cytochrome b5 and cytochrome b5 reductase during senescence of erythrocytes: relation to the increased methemoglobin content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsVWiu7o%3D&md5=b38492c110ec6f3f87a1974364de4a23CAS | 6874674PubMed |
Vacha J, Znojil V (1981) The allometric dependence of the life span of erythrocytes on body weight in mammals. Comparative Biochemistry and Physiology Part A: Physiology 69, 357–362.
| The allometric dependence of the life span of erythrocytes on body weight in mammals.Crossref | GoogleScholarGoogle Scholar |
van Kampen E, Zijlstra WG (1961) Standardization of hemoglobinometry. II. The hemiglobincyanide method. Clinica Chimica Acta 6, 538–544.
| Standardization of hemoglobinometry. II. The hemiglobincyanide method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXhsVCktb8%3D&md5=19bcec8dfdc854f03912cd4ddcf672d6CAS |
van Zijderveld SM, Gerrits WJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA, Perdok HB (2010) Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. Journal of Dairy Science 93, 5856–5866.
| Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1Kis7Y%3D&md5=2c90a9348249f958588d724bd6912c2aCAS | 21094759PubMed |
van Zijderveld SM, Gerrits WJ, Dijkstra J, Newbold JR, Hulshof RB, Perdok HB (2011) Persistency of methane mitigation by dietary nitrate supplementation in dairy cows. Journal of Dairy Science 94, 4028–4038.
| Persistency of methane mitigation by dietary nitrate supplementation in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsVylur4%3D&md5=b403e5eac8ed8ca1f5a91dddfa81918fCAS | 21787938PubMed |
Vetrella M, Astedt B, Barthelmai W, Neuvians D (1971) Activity of NADH- and NADPH-dependent methemoglobin reductases in erythrocytes from fetal to adult age. A parallel assessment. Klinische Wochenschrift 49, 972–977.
| Activity of NADH- and NADPH-dependent methemoglobin reductases in erythrocytes from fetal to adult age. A parallel assessment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXlt1Oltrw%3D&md5=174babeba6c075e2a8215827b39f74e8CAS | 4398423PubMed |
Wegener G, Krause U (2002) Different modes of activating phosphofructokinase, a key regulatory enzyme of glycolysis, in working vertebrate muscle. Biochemical Society Transactions 30, 264–270.
| Different modes of activating phosphofructokinase, a key regulatory enzyme of glycolysis, in working vertebrate muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVKgs7k%3D&md5=0b8a3d49792ccd11c52766aa47f050b3CAS | 12023862PubMed |